Estimating population characteristics of two saproxylic beetles: a mark ...

J Insect Conserv (2011) 15:401–408 DOI 10.1007/s10841-010-9313-3

ORIGINAL PAPER

Estimating population characteristics of two saproxylic beetles: a mark-recapture approach Tuuli Tikkama¨ki • Atte Komonen

Received: 28 December 2009 / Accepted: 12 July 2010 / Published online: 22 July 2010 Ó Springer Science+Business Media B.V. 2010

Abstract Using a mark-release-recapture technique we describe adult sex ratios, recapture rates and other sample characteristics of two saproxylic species: the nationally threatened longhorn beetle Leptura (Rutpela) maculata (Coleoptera: Cerambycidae) and the common L. quadrifasciata in southeastern Finland over two summers. Over 350 individuals of L. maculata and 150 individuals of L. quadrifasciata were captured on floral resource or in flight, and marked each summer. For L. maculata, the sex ratio was male-biased (2:1), whereas for L. quadrifasciata the bias was less clear. For both species, the male-bias may reflect behavioral differences between sexes, rather than true population differences. The proportion of recaptured individuals was low and varied between 7 and 33% depending on the species and year, which allowed us to estimate population parameters only for L. maculata in 2006. A model which assumed constant survival, but timedependent catchability and entrance probability from a larger superpopulation, fit the data best. The precision of the total population size estimates were reasonable for all the models tested (coefficient of variation = 7–14%). Based on the estimated local adult population size (mean ± 95% confidence interval = 865 ± 131), and the current distribution area of L. maculata, we infer that the species is not in immediate risk of extinction in Finland. Our analysis shows that mark-recapture technique can provide precise estimates of adult population size of T. Tikkama¨ki Natural Heritage Services, Metsa¨hallitus, Yla¨-Kolintie 22, 83960 Koli, Finland A. Komonen (&) School of Forest Sciences, University of Eastern Finland, P.O. Box 111, 80101 Joensuu, Finland e-mail: [email protected]

saproxylic beetles which have different adult and larval habitats, and thus be useful in assessing extinction risk and monitoring population trends. Keywords Cerambycidae Coleoptera Population size Saproxylic Threatened species

Introduction In forest ecosystems, many of the threatened beetle species are saproxylic, i.e. they are dependent on dead wood. To assess the extinction risk of these species, and to develop monitoring measures, quantitative information on population size, structure, and dynamics are urgently needed (Komonen et al. 2008). Unfortunately, population data for saproxylic beetles are particularly hard to obtain, because the adults are difficult to detect and count data from different trapping schemes are difficult to link with population size. Consequently, numerical studies on threatened saproxylic beetles have been largely restricted to counts of larvae (Siitonen and Saaristo 2000; Martikainen 2002), or to counts of emergence holes of adults (Wikars 2004; Buse et al. 2008). Such indirect studies provide useful information regarding the substrate and habitat requirements of the target taxon, but direct data on adults may be more useful in monitoring populations and fully evaluating the extinction risk. In addition to practical problems in sampling larval habitat (destructive) and adult emergence holes (species identity), many population characteristics of conservation importance (e.g. effective population size, sex ratio) can only be studied with adults. In species whose adults can be easily captured and marked, the mark-release-recapture (MRR) approach is a priori suitable for quantifying population characteristics

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(Amstrup et al. 2005). MRR has been used to estimate adult population size of saproxylic ‘pest’ species, such as some bark beetles (Weslien and Lindelo¨w 1989) and longhorn beetles (Shibata 1986). MRR studies on non-pest saproxylic beetles are scarce, and they share one common feature, namely that the larval and adult habitat coincide (tree hollows, Ranius 2002; fungal sporocarps, Whitlock 1992; Nilsson 1997b; Starzomski and Bondrup-Nielsen 2002). Extant studies demonstrate that the MRR approach to estimate population characteristics does work with such saproxylic beetles. However, the very habitat shared by the larvae and adults can be expected to correlate with sedentary adult behavior, because adults do not need to disperse to seek for forage (Hanks 1999; Ranius 2006). Similarly, saproxylic beetles occupying the ephemeral and unpredictable subcortical habitat are likely to be more mobile than species occupying persistent habitats, such heart and sap wood (Hanks 1999) or wood mould in tree hollows (Ranius 2006). High daily activity and frequent long-distance movements can be expected to reduce the capture and recapture probabilities, and consequently the applicability of the MRR technique to estimate population characteristics. This makes generalization across ecological groups difficult, and one must empirically establish the suitability of the MRR approach to different saproxylic beetle species. We wanted to find out whether MRR could be used in evaluating population characteristics of two saproxylic longhorn beetles for which larval and adult habitats do not coincide, and which develop in decaying wood and are thus likely to fall in between the extremes in terms of habitat longevity and predictability. Our study species were the nationally threatened Leptura maculata (Coleoptera: Cerambycidae) and the common L. quadrifasciata in Finland. For both species, the larval habitat (dead wood in forests) and the adult habitat (floral resource in meadows and road verges) do not generally overlap. We present results on species biology based solely on marked individuals, and provide formal estimates of population size for L. maculata.

Materials and methods Study species The northernmost European population of Leptura (Rutpela) maculata Poda 1761 occurs in the Puumala region in southeastern Finland, which is also its only known region of occurrence in Finland (Bense 1995; Helio¨vaara et al. 2004). In Finland, the species is considered a climatic relict (Komonen 2007), and it is classified as vulnerable following the IUCN red list criteria (Rassi et al. 2001); Leptura quadrifasciata Linnaeus 1758 is a widespread species.

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In Finland, L. quadrifasciata develops in logs, snags, fallen branches and stumps of birch (Betula spp.), alder (Alnus spp.) and aspen (Populus tremula) at varying decay stages and with diameter C 10 cm, usually at moist sites (Helio¨vaara et al. 2004). The host plants of L. maculata are not known, but are supposed to be birch or alder. The larval and pupal development of both species takes 2–3 years. The adult body size (body length = 14–19 mm) is similar for both species, and females are slightly larger than males. Adults are diurnal and can be seen on flight on July and early August when they are foraging and mating on flowers, mainly of Angelica sylvestris and Filipendula ulmaria, and can easily be detected and captured. Because these plants favor open areas, the larval and adult habitats do not generally overlap. Sampling The study was conducted in the Puumala region (61°290 N, 28°130 E) in south-eastern Finland from 12th July to 3rd August 2005 and from 9th July to 3rd August 2006, which coincides with the activity period of adults. The region is a mosaic of managed forests, agricultural fields and lakes. Twelve percent of the forest area is broadleaf-dominated or mixed forests, 3% of all forests is over 120 years old, and the average amount of dead wood of broadleaved trees is about 1 m3/ha (Anon. 2009). The study was conducted at three sites which were all parts of continuous habitat. The main MRR (Site 1) was conducted along both verges (each ca. 4 m wide) of a 1.2 km stretch of a road, and flowers of A. sylvestris, F. ulmaria, Epilobium angustifolium and other large-sized flowering plants were searched for the beetles; beetles were also caught in flight. Beetles were marked with individual codes on the pronotum and elytra using permanent silver and gold ink pens. For each beetle, we recorded sex, time of capture and GPS coordinates (only in 2006). Marked beetles were carefully released back onto flowers on which they either stayed or they dropped to the ground. Site 1 was sampled by the same person roughly at the same time of the day (10:00–15:00). A sampling occasion lasted on average 105 min. Only recaptures between sampling occasions (days) were taken into account in analyses. To get some ground for generalization, we conducted MRR at two additional sites in 2006, but for a shorter period of time (16th of July to 3rd of August) and using site-, not individual-specific markings (thus population parameters cannot be reported). The length of site 2 was 830 m (width of each verge ca. 2 m) and the length of site 3 was 700 m (verge width ca. 4 m). These sites were sampled by the same person between 10:30 and 15:00, and the sampling occasion lasted on average 47 and 54 min at the sites 2 and 3, respectively. To evaluate daily dynamics,


site 2 was sampled three times (10:05, 12:15, 14:45) on the 25th of July in 2006. Mark-release-recapture analyses To estimate the population size of L. maculata, we used the POPAN formulation of the Jolly-Seber model as implemented in the MARK software (vers. 5.1; White 2009). The model is an open population model, which allows for births, deaths, and migration. The Jolly-Seber model has the following main assumptions: (1) every marked individual present in the population at time (i) has the same probability of recapture (pi); (2) every marked individual in the population immediately after time (i) has the same probability of survival to time (i ? 1); (3) marks are not lost or missed; and (4) all samples are instantaneous, relative to the interval between occasion (i) and (i ? 1), and each release is made immediately after the sample (Amstrup et al. 2005). Although capture rates (assumption 1) and survival (assumption 2) can differ between males and females, the sample size did not warrant analysis by sex. In MARK, the RELEASE program provides goodnessof-fit-tests, which can be interpreted to test assumptions 1 and 2 (see ‘‘Results’’). Sampling occasion was short (few hours) relative to the interval between occasions (1 day at a minimum) (assumption 4), but we have to assume that marks were not lost (assumption 3). The model consists of three primary parameter groups: one group describes the survival probability (u), another the capture probability (p) and a third group the probability of entrance (b) from a larger superpopulation. The term entrance refers to any new individual that immigrates from outside the sampling site, and thus it reflects both birth dynamics as well as movement from the place of birth to the feeding and mating sites. A superpopulation can be interpreted as the total number of beetles ever present in the study area between the first and last sampling occasion. The parameters derived are daily (Ni) and superpopulation size (Ntot). We modeled the survival and capture probabilities using a logit link function, the entrance probability using a multinomial logit link function (these probabilities sum up to 1), and the population size using a log link function. The mean survival (u0 ) and catchability (p0 ) are arithmetic means from estimated daily values. The mean residence time was derived from -ln(u0 )-1. Because weather prohibited sampling during certain days, we adjusted the analyses for the unequal time periods between sampling occasions. We first evaluated the goodness-of-fit, as implemented in RELEASE, of the fully time dependent model (utptbt), i.e. a model where the probability of survival, capture and entrance all vary from one sampling occasion to another. Because this model adequately fit the data (see ‘‘Results’’), we then proceeded

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to test simpler models, i.e. relaxing the time-dependence of survival and/or capture probability. These different models were compared using Akaike’s Information Criterion corrected for small sample bias (AICc).

Results Marked individuals At all sites, the total number of marked individuals was larger for L. maculata than for L. quadrifasciata (Table 1). At site 1, the proportion of recaptured individuals of L. maculata was higher than for L. quadrifasciata, and for both species the number of marked individuals and the rate of recapture were higher in 2006 than 2005. There was also a clear difference in the number of individuals recorded over the seasons of 2005 and 2006: a clear peak in abundance was reached only in 2006 (Figs. 1, 2). Of the recaptured L. maculata, 78 and 70% were recaptured only once (max = 6 times), and the mean time between recaptures was 6.7 (max = 20) and 5.4 (max = 24) days in 2005 and 2006, respectively. Of the recaptured L. quadrifasciata, 80 and 79% were recaptured only once (max = 2), and the mean time between recaptures was 3.6 (max = 6) and 4.3 (max = 15) days in 2005 and 2006, respectively.

Table 1 Total number of marked individuals and the percentage of recaptured individuals (in parentheses) of Leptura maculata and L. quadrifasciata in the three study sites Lepmac

Lepqua

208 (25)

40 (5)

Site 1 (2005) Males Females

108 (10)

53 (8)

Totala

383 (19)

139 (7)

232 (38)

83 (18)

Site 1 (2006) Males Females

123 (22)

52 (29)

Totala

355 (33)

151 (17)

Males

66

20

Females

33

9

Totala

106

47

Males

74

49

Females

42

41

Totala

119

114

Site 2 (2006)

Site 3 (2006)

Sampling period varied between years and sites; see main text for details a

Includes individuals for which sex was not determined

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Fig. 1 The number of marked and recaptured individuals of Leptura maculata and L. quadrifasciata at the main study site 1 from 12 July to 3 August 2005 and from 9 July to 3 August 2006

Fig. 2 The number of marked and recaptured individuals of Leptura maculata and L. quadrifasciata at the sites 2 and 3 from 16 July to 3 August 2006

Although intensive sampling was done at site 1 only, the density (per 100 m) of L. maculata at this site (30 individuals) was similar to those at sites 2 (25) and 3 (34), based on the assumption that similar proportions of the total catch were obtained before the 16th of July as at site 1; these densities should not be taken as formal estimates of population density. The resurveys that were conducted twice during 1 day at site 2 demonstrated that the proportion of marked individuals varies during the day: 27 (40% marked) L. maculata individuals were observed in the first, 25 (48%) in the second, and 12 (67%) in the third survey.

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The respective figures for L. quadrifasciata were 5 (20% marked), 8 (0%), and 1 (0%) individuals. The sex ratio was male-biased: 66% (variation between sites = 64–67%) of L. maculata and 57% (43–69%) of L. quadrifasciata were males (Table 1). The male-bias was also consistent over the season (Fig. 3). For L. maculata, the proportion of recaptured male individuals was higher than that of females, and 86% (2005) and 83% (2006) of the individuals that were recaptured more than once were males. For L. quadrifasciata, the proportion of recaptured males was lower than that of females, yet 67%


405

After the population peak, the daily estimates were also relatively precise, as illustrated for the best fit model (u.ptbt) (Fig. 4b). According to this constant survival model, the overall population size was estimated to be 865 (95% confidence interval = 734–996; Table 2). The relative precision of the total population size estimates was reasonable (coefficient of variation = 7–14%) for all the models: the models which assumed a constant survival probability had the narrowest confidence intervals. Average daily catchability (p0 ) was 15% (min–max = 7–25%) and survival (u0 ) 86% (min–max = 26–100%), but many of the daily estimates were very imprecise. The mean residence time was estimated to be 7 days. Fig. 3 Dynamics of daily sex ratio for Leptura maculata and L. quadrifasciata at site 1 in 2005 and 2006

Discussion Population size

(2006) of the individuals that were recaptured more than once were males; in 2005 only one individual was recaptured more than once. For both species, males moved more actively along the road verges than females, the mean distance travelled by an individual being 296 m (max = 2,572) and 137 m (max = 1,083) during the sampling period, respectively. Population parameters Our data was adequate to estimate population parameters only for L. maculata in 2006. The model which assumed a constant survival (u.) and time-dependent capture probability (pt) clearly outperformed the other models (Table 2). Those models that assumed a constant entrance probability (b.) from the superpopulation did not fit the data at all, and thus they are not reported. The estimated mean daily population size and trend over the season were rather similar for the four models (Fig. 4a).

Somewhat surprisingly, the threatened L. maculata was consistently more abundant than the widespread L. quadrifasciata. Because we do not know the larval host plants of L. maculata, it is impossible to explain the difference in population size. For L. maculata, the formal estimates of local population size (700–1,300 individuals), coupled with the known area of occupancy (ca. 100 km2), imply that the total Finnish population size is over 10,000 individuals. This is clearly more than needed to avoid the imminent extinction due to demographic and genetic stochasticity (e.g. Boyce 1992). The population size estimates and their precision, using the four different models, were very close to each other and all had relatively small coefficients of variation. According to the precautionary principle in conservation biology, it is generally better to under- than overestimate the population size. In MRR, population size estimates often tend to be too small due to heterogeneity of capture probabilities (Pollock et al. 1990; Ranius 2001), so

Table 2 Comparison of the four models that were used to estimate the population size (Ntot) of Leptura maculata in 2006 Modela

AICc

DAICc

Number of parametersb

Ntot

95% confidence intervals

CV (%)c

u(.)p(t)b(t)

1,367

0.0

37

865

734

996

8

u(t)p(t)b(t)

1,382

15.7

51

993

715

1,270

14

u(t)p(.)b(t)

1,397

31.2

36

989

723

1,254

14

u(.)p(.)b(t)

1,401

34.0

20

886

763

1,009

7

Comparison is based on Akaike’s Information Criterion corrected for small sample bias (AICc), DAICc indicating the difference between the models. u = survival probability, p = capture probability and b = entrance probability from a larger superpopulation; (.) indicates constant probability and (t) time-dependent probability a

Goodness-of-fit of the fully time-dependent model u(t)p(t)b(t): v2 = 39.2, df = 54, p = 0.93; Test 2 and Test 3: v2 = 20.6 & 18.6, p = 0.80 & 0.88, respectively, df = 27

b

u(t)p(t)b(t) has 3k-3 parameters (k = sampling occasions), because not all parameters are identifiable

c

Coefficient of Variation is the standard error divided by Nest, and indicates the precision of the population size estimate

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Fig. 4 The mean estimated daily population size of Leptura maculata at site 1 from 9 July to 3 August 2006, using four different models (a), and the model u(.)p(t)b(t), which got the strongest support according to AICc (b). u, p and b represent the probability of

survival and capture, as well as the probability of entrance from the larger superpopulation, respectively; (.) indicates a constant probability through time, whereas (t) indicates a time-dependent probability. Error bars indicate 95% confidence intervals

in many cases these estimates are likely to be in accordance with the precautionary principle. Furthermore, the density of L. maculata over the study sites was similar, which provides numerical support for our field experience that the main study population was not exceptionally large. Future research should establish the host plant requirements of L. maculata, and then link habitat availability and dynamics with population size using MRR. Our general research target was to test if MRR approach is suitable for estimating population parameters of saproxylic beetles for which larval and adult habitats do not coincide. Our study demonstrates that it is possible to obtain adequate data for population estimates, but the outcome may be highly time and place dependent, as has previously been demonstrated for saproxylics (Ranius 2001), as well as for other insects (Harker and Shreeve 2008). The general problem in using MRR approach with insects is that even in intensive field surveys only a small proportion of individuals may be recorded and the recapture rate tends to remain low (Hanks et al. 1998; Ranius 2002). The failure to estimate parameters precisely, however, does not necessarily imply a complete failure: the numbers and characteristics of marked individuals can unravel key features of a species’ ecology, as we also show here, and be useful in red-list assessment and population monitoring.

L. quadrifasciata seems to be similar to other flowerfeeding cerambycids (Hanks 1999). The overall recapture rates were rather low. To some extent this was expected, because predictability and co-occurrence of both larval and adult resources apparently links with sedentary behavior in saproxylic beetles (Shibata 1986; Hanks 1999; Ranius 2001; Nilsson 1997b), whereas if larval and adult habitats do not co-occur, beetle activity is likely to be greater (Hanks et al. 1998; Hanks 1999). The low recapture rate is likely explained by both the active turnover of the population in the road verges, and that only a small proportion of the individuals present is detected and marked during a survey occasion; there is some support for both of these explanations based on the resurveys that were conducted at one site over a day.

Survival and recapture rates The mean survival and residence time estimates were similar to those documented for other saproxylic cerambycids (Shibata 1986, 1994). However, the data were not adequate to estimate daily survival precisely. Because the survival estimate included emigration, it is naturally an underestimate and cannot be used to assess longevity directly; nevertheless, based on the maximum time between captures the longevity of both L. maculata and

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Population dynamics At site 1, the total number of marked individuals for both species in both years was similar even though the weather was colder and rainier in July 2005 than in 2006 (with 4 and 12 days above ?25°C, respectively; data from Finnish Meteorological Institute). It is impossible to say anything about long-term fluctuations in the studied species, but our results do not contradict previous studies that have demonstrated that saproxylic beetles seem to fluctuate irrespective of yearly weather conditions (Nilsson 1997a; Ranius 2002). If weather-dependent population fluctuations turn out to be weak for saproxylic beetles generally, then this will lower their risk of extinction. The weather apparently influenced the recapture rate and within-season population dynamics. In the cooler year (2005), the recapture rate was lower, the peak in abundance was reached later and the activity period, i.e. mating and feeding on flowers, was prolonged in comparison with 2006. At all sites, the daily population sizes were skewed to the right, i.e. the peak was reached rather quickly and then


started to gradually fade away, in a similar way to many other beetles (Koji and Nakamura 2006; Shibata 1981; Hanks et al. 1998; Smith et al. 2004). In this study, the end of the flight activity coincided with the senescence of the adult food plants; thus, it is impossible to say whether the beetles died out or simply moved into the forest. Differences between sexes The two study species showed somewhat different patterns in terms of sex ratios and in the behavior of males and females. For L. maculata, the pattern was very clear and consistent between sites and years: more males were marked and recaptured (in absolute and relative terms) than females; and males were also more frequently recaptured several times than females. For L. quadrifasciata, the difference was less consistent, but the proportion of individuals for which sex was not determined was high and the recapture rate low, especially in 2005. The documented male-biased sex ratio can be taken as typical for cerambycids in field samples (Shibata 1986, 1994; Hanks et al. 1998; Smith et al. 2004). Higher recapture probabilities for males have been found also in other insects (Kuussaari et al. 1996; Stoks 2001; Roslin et al. 2009), including saproxylic beetles (Ranius 2001). Male-biased sex ratio in captures and recaptures does not necessarily reflect population difference. In saproxylic cerambycids, males are generally more active in locating mates than females (Hanks 1999). Also in our study, males were more often captured in flight, and they moved on average more than females. Females are also likely to move from floral resource to lay eggs, whereas the polygynous males should remain in the foraging habitat to locate mates. This is supported by the higher probability of males being recaptured. The higher activity and catchability of males, and the consequent male-biased sex ratio in field samples of insects has been widely discussed (Adamski 2004; Stoks 2001). If male-biased sex ratio is only an artifact, then the true population size would actually be larger than the one estimated here, because sexes were not analysed separately and thus female population size was underestimated. Implications for conservation Our results show that it is possible to obtain precise estimates of population size in saproxylic beetles for which larval and adult habitat do not coincide. In monitoring population trends, however, there are several points that have to be kept in mind. First, the within-season dynamics are very clear (see also Smith et al. 2004), which means that any monitoring has to extend over the entire flight period, because the population peak is influenced by

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weather and thus hard to predict. Second, weather also influences the daily variation in population size (even if rainy days are excluded), and during the peak flight period two consecutive days can differ in the number of individuals by over 100%. This means that obtaining comparable data from many sites require substantial working power, especially since the daily time window for sampling is only a few hours (see also Hughes and Hughes 1982). Third, long-term population dynamics of saproxylic beetles are poorly understood, and thus MRR should preferably be conducted over many years. Reliable estimation of population size, structure and dynamics are needed to answer many fundamental ecological questions. Unfortunately, the understanding of population characteristics of saproxylic beetles is poor at its best, and largely based on anecdotal observations, rather than on systematic studies (Komonen et al. 2008). For L. maculata, our results imply that the Finnish population size is more than the threshold for red-listing under the population size-related criteria (C and D) of the IUCN protocol (IUCN 2001). If L. maculata really is a climatic relict and its occurrence is not restricted due to lack of suitable substrates (Komonen 2007), then the species is also likely to expand its range along with warming climate. In conclusion, our study clearly demonstrates the applicability of MRR in providing ‘‘hard data’’ for red-list assessment (see also Ranius 2007; Roslin et al. 2009). Although the population size-related criteria are inherently less applicable in red-list assessment of invertebrates than range size-related criteria, population size is yet a fundamental determinant of extinction risk, and needed, for example, for a population viability analysis. Thus, empirical tests of the mark-release-recapture approach deserve further attention in saproxylic insects. Acknowledgments We thank Suomen Hyo¨nteistieteellinen Seura, Suomen Biologian Seura Vanamo and Finnish Environment Institute for financial support. Thomas Ranius and Tomas Roslin gave valuable comments on an earlier version of the manuscript.

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